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1
Effects of Age on Speech Understanding in Normal Hearing Listeners:
Relationships Between the Auditory Efferent System
and Speech Intelligibility in Noise
SungHee Kima,c , Robert D. Frisinaª,b.c and D. Robert Frisinac,a
aOtolaryngology Division, bDepartments of Surgery, Neurobiology &Anatomy and Biomedical Engineering, University of Rochester School of Medicine and Dentistry, and cInternational Center for Hearing and Speech Research, National Technical Institute for the Deaf, Rochester Institute of Technology, Rochester NY, USA Key words: Aging, Presbycusis, Olivocochlear bundle, Medial Efferent System,
Hearing-in-noise, Speech perception
emails: [email protected], [email protected], [email protected]
Corresponding Author: Robert D. Frisina, PhD Otolaryngology Assoc. Chair University of Rochester School of Medicine 601 Elmwood Avenue Rochester, NY 14642-8629, USA Phone: 585-275-8130 FAX: 585-271-8552 e-Mail: [email protected]
2
ABSTRACT Human listeners are able to concentrate on listening to one voice amidst other
conversations and background noise, but not all of the neural mechanisms for this process
are understood. There is growing evidence in normal-hearing subjects that the medial
olivocochlear (MOC) auditory efferent system is involved in the detection of signals in
noise, such as speech sounds, by modulation of cochlear active physiological
mechanisms. The present investigation aimed to evaluate the MOC efferent involvement
in speech intelligibility in noise and spatial release from masking (RFM) in normal-
hearing adults of different ages. Contralateral suppression (CS) of distortion product
otoacoustic emission was used to measure MOC efferent system function. Using HINT
(Hearing in the Noise Test), we measured speech intelligibility in noise at 0 degree
azimuth (HINT N0) and the improvement of speech intelligibility in noise, i.e. release
from masking (RFM), when speech and noise were spatially separated. Correlation
analysis was applied to reveal relations between the MOC efferent system, speech
intelligibility in noise and spatial RFM. The findings suggest: (1) age-related difficulty
understanding speech in background noise is related to an age-related functional decline
of the MOC efferent system, (2) the higher frequency (4-6 kHz) range of the MOC
efferent function is correlated with speech processing in background noise, and (3) the 1-
2 kHz frequency range of the MOC efferent system is correlated with a spatial RFM, i.e.,
“cocktail party” processing capability based on binaural hearing. In conclusion, the
MOC efferent system can be characterized as a nonlinear adaptive filter activated during
speech processing in background noise and also as a cocktail party processor.
3
I. INTRODUCTION
In realistic acoustical environments where various sounds reach our ears
simultaneously, we can listen adaptively to a particular sound in the mixture of sounds by
focusing our attention on it. This phenomenon is known as the “cocktail party” effect
(Cherry, 1953; Yost, 1997). Physiological correlates of this effect have not been
extensively studied yet. To date, no computer systems have had such an effective
adaptive sound selection mechanism, even though many signal processing studies have
been conducted on this topic (Giguere and Woodland, 1994; Cooke and Ellis, 2001;
Rouat and Pichevar, 2002).
There is growing evidence in normal hearing young adult subjects that the
auditory medial olivocochlear (MOC) efferent system is involved in the detection of
signals in noise (Micheyl et al., 1995; Micheyl and Collet, 1996), including signals such
as speech sounds (Giraud et al., 1997; Zeng et al., 2000), by modulation of the cochlear
active mechanisms. However, the full extent of the MOC system’s role in hearing is still
not well understood. Several hypotheses have been proposed for an efferent involvement
in anti-masking (e.g., Winslow et al., 1987; Kawase et al., 1993a,b; Micheyl et al., 1995;
Giraud et al., 1997; Heinz et al., 1998; Liberman 1988; Liberman and Guinan, 1998),
protection from damage due to loud noise (Cody and Johnstone, 1982; Handrock and
Zeiberg, 1982; Rajan 1990; Liberman and Gao, 1995), auditory and visual attention
(Igarashi et al., 1974; Oatman, 1976; Scharf et al., 1994, 1997), and auditory
development (Walsh et al., 1998) and degeneration with age (Kim et al., 2002). Among
these hypotheses, the anti-masking effect has received the most extensive investigation,
4
and probably has the strongest empirical support. This effect is most likely mediated
through MOC innervations to the outer hair cells (OHCs).
Otoacoustic emissions (OAEs) are thought to be by-products of cochlear active
mechanisms, i.e., the motility of OHCs (Kemp, 1978; Brownell et al., 1985). Since Buño
(1978) and Murata’s work (1980) showing that acoustical stimulation of one cochlea can
modify the firing of afferent fibers in the contralateral cochlea, experiments have
indicated the feasibility of studying the MOC’s activity non-invasively by presenting
contralateral stimulation during OAE recordings (Littman et al., 1992; Williams et al.,
1994; Maison et al., 1997; Micheyl and Collet, 1996).
Recently, Kim et al. (2002) demonstrated that the function of the MOC efferent
system declines with age in human listeners with normal audiometric thresholds. MOC
efferent strength was measured by contralateral suppression (CS) of distortion product
otoacoustic emissions (DPOAEs) with a wideband noise. They found that the CS declines
at an earlier age than the age-dependent decrease in DPOAE amplitudes.
It has long been known that the elderly with and without hearing loss have more
difficulty in understanding speech than young listeners, especially in background noise
(CHABA, 1988). However, the exact relationship between speech recognition
performance and chronological age has not yet been determined, due to the combined
effects of peripheral hearing loss and age-related changes in the brain. Recently Kim et
al. (2003) studied the effect of age on binaural speech intelligibility in noise in normal
hearing subjects, using HINT (Hearing in Noise Test). Their findings suggested that age
degrades speech intelligibility in both quiet and noise. In addition, benefit from spatial
separation of speech and noise, i.e., spatial release from masking (RFM), declined with
5
age. This RFM is probably one brainstem auditory system mechanism that contributes to
the “cocktail party effect” as one aspect of sound source determination.
The purpose of the present investigation was to evaluate the MOC auditory
efferent involvement in speech intelligibility in noise and spatial RFM, in normal hearing
human listeners of different ages.
II. METHODS
Subjects
This study was performed with 25 subjects, 18 to 75 years old. Table 1
summarizes the ages of the subjects who were classified as young (16 to 30 years old),
middle aged (38 to 52 years old) and old (greater than 60 years old). Their otological
histories indicated that they were clear of factors such as drug ototoxicity, long-term
noise exposure, or ear infections. A battery of hearing tests was completed in order to
establish integrity of their auditory systems. Pure tone audiometry was performed in a
sound-proof room, using a Grason-Stadler GSI 61 clinical audiometer, at frequencies
between 0.25 kHz and 8 kHz (0.25, 0.5, 1, 2, 4, 6, and 8 kHz). All subjects had pure tone
thresholds of 20 dB HL or better for standard audiometric frequencies up to 4 kHz (Fig.
1). They showed symmetric hearing within 10 dB. The target ear for assessing MOC
function was the better ear as determined by pure tone audiometry.
6
Assessment of the MOC system function
The strength of the MOC auditory efferent system was evaluated by CS,
according to the method utilized by Kim et al. (2002). CS was calculated by subtracting
the DPOAE amplitude without noise from those with contralateral wide band noise
(WBN). The reduction in DPOAE amplitude due to the presence of contralateral noise
(CS) was presented as negative value.
All DPOAEs were recorded using an ILO 92 Otodynamics Ltd. Analyzer.
Throughout the measurements, the ratio of f2/f1 was fixed at 1.22. The stimulus levels
were held constant, at L1=75 dB SPL and L2=65 dB SPL. The 2f1-f2 DPOAE amplitude
as a function of frequency was recorded at four points per octave to obtain a wideband
response in the 1 to 6-kHz range. DPOAE amplitude was measured for each frequency.
Contralateral acoustic stimulation was a 30 dB SL wideband noise, which was generated
by a Grason-Stadler GSI 61 clinical audiometer and applied via a 3A insert ear phone.
All measurements were done in an IAC sound-proof room with the subject seated
in an armchair comfortably and relaxed throughout the test session, which lasted for
approximately 30 min. Each test session consisted of three initial DPOAE measurements
without noise followed by three measurements with contralateral WBN exposures at 30
dB SL. WBN was presented 15 seconds prior to the beginning of the DPOAE stimulus
and continued until the DPOAE measurement was completed.
Assessment of the speech intelligibility
7
To assess speech intelligibility, we performed the hearing in noise test (HINT).
HINT (Nilsson et al., 1994) was developed to provide a reliable and efficient measure of
speech reception thresholds for sentences (sSRT). Also, the free field and background
noise conditions of HINT provide an opportunity to get closer to real-life listening
situations.
Speech materials (sentences) were always presented at 0° azimuth. Sentence lists
were presented in the following conditions according to HINT instructions: (1) speech in
65 dB(A) noise at 0° azimuth (HINT N0), (2) speech in 65 dB(A) noise at 90° azimuth
(HINT N90), (3) speech in 65 dB(A) noise at 270° azimuth (HINT N270). The subject
was seated approximately 1 meter equidistant from three loudspeakers in a double-walled
sound booth.
An adaptive procedure (Levitt, 1971) without feedback was used to determine the
50% point on the psychometric function required for speech recognition thresholds. The
beginning intensity level of speech was 61 dB(A) and the noise channel was turned on
and remained at 65 dB(A). Noise onset preceded each sentence by 1 second and was
turned off 1 second after each sentence was completed. The first sentence in each list of
sentences was repeated at increased levels until identified correctly. The intensity level of
speech then was decreased by 4 dB and the second sentence presented. Stimulus level
was raised (incorrect response) or lowered (correct response) by 4 dB after subject’s
responses to the second and third sentences. The step size was reduced to 2 dB after three
sentences, and a simple up-down stepping rule was continued for the remaining 17
sentences. The calculation of the signal-to-noise ratio (SNR) for 50 percent sentence
8
recognition was based on averaging the presentation levels of sentences 4 through 20 for
the test list.
In this study, we evaluated speech intelligibility in noise using SNR of HINT N0
and RFM using an average SNR improvement of the HINT N90 and HINT N270
conditions relative to the HINT N0 condition.
All methods have been approved by our human subjects institutional review
boards and have been conducted according to the principles of the Declaration of
Helsinki.
Data Analyses
From the DP-gram, CS was obtained for the 1-6 kHz frequency range for f2. To
evaluate the effect of different frequency ranges, we arbitrarily divided the full frequency
range into 1-2 kHz and 4-6 kHz frequency ranges. To reveal the MOC auditory efferent
functional involvement in the cocktail party effect, different frequency ranges of CSs
were compared with HINT N0 and RFM using correlation analysis. To evaluate the age
effect on speech understanding in noise, age was also made comparisons between the
HINT N0 and RFM.
III. RESULTS
Table 2 showed average CS in the different frequency ranges for each age group.
And Table 3 showed the results of speech intelligibility of HINT N0 and speech
intelligibility gain when speech and noise were spatially separated (RFM).
9
The average CS in the higher frequency (4-6 kHz) range is correlated with HINT
N0 (Pearson r=0.4295, p<0.05), as shown in Fig. 2. Note that the greater the strength of
the MOC efferent system, the more negative the value of the CS. A zero or positive CS
value means that there was no change or there was an enhancement of the DPOAE
amplitude, respectively, when the contralateral noise was applied. The relative amplitude
of the CS in the 4-6 kHz ranged from –1.97 to 1.62 dB. The SNR of HINT N0 ranged
from –0.8 to –4.4 dB. Every subject within normal hearing level performed 50 % correct
speech intelligibility at less than noise level, i.e., negative SNR. According to HINT
procedural conventions, the wideband noise was fixed at 65 dB(A). The speech reception
thresholds for sentences in the background noise at 0 degree azimuth ranged from 61.6 to
64.2 dB(A).
Fig. 3 shows that the average CS in the 1-2 kHz frequency range was correlated
with the RFM (Pearson r=-0.4455, p<0.05). The relative amplitude of CS in the1-2 kHz
bandwidth ranged from –1.99 to 0.94 dB. The RFM is the improvement of speech
intelligibility in noise resulting from the spatial separation of the noise speaker from the
speech speaker at N0. The range of RFM was found to be from 1.80 to 7.55 dB. The
larger the RFM, the greater the benefit in speech understanding in background noise
resulting from moving the noise source away from the speech source.
Age was found to be correlated with the HINT N0 thresholds and the RFM
measurements (Pearson r=0.5470, p<0.01, and Pearson r=0.4059, p<0.05, respectively).
10
IV. DISCUSSION
Using the HINT test, speech intelligibility in noise was measured using an
adaptive procedure to determine the SNR for 50% intelligibility. The SNRs typically
obtained are in the range of –2 to -5 dB (Glasberg and Moore, 1989; Plomp, 1994) when
the background sound is a steady noise with the same long-term average spectrum of
speech (called speech-shaped noise). Even though SNR differences are not large in terms
of dB, a 1dB improvement of SNR improves speech intelligibility by 11% to 19 %
(Plomp and Mimpen, 1979; Laurence et al., 1983; Moore et al., 1992; Nilsson et al.,
1994).
The HINT N0 condition is one in which speech and noise are presented binaurally
with no interaural differences. In the present study it was found that the CS in the 4-6
kHz frequency range is statistically correlated with SNR for HINT N0. This finding
suggests that the higher frequency range of the MOC efferent system function is related
with speech processing when the background noise and speech come from similar
locations. In a real listening environment, though, it is hard to have identical sound
sources (distance and azimuth of the signal and noise).
Cherry (1953) coined the term “cocktail party effect” to describe the auditory
system’s ability to determine the sources of sounds in a multi-source acoustical
environment. In psychophysical terms, signal detection and speech perception improve
when the target and competing noise are spatially separated, thereby demonstrating the
advantage provided by binaural hearing. However not all the neural mechanisms for this
process are completely understood.
11
Spatial RFM is the measured improvement of speech intelligibility when spatially
separating a signal from the background noise. The CS in the 1-2 kHz frequency range
was statistically correlated with this spatial RFM in the present investigation. This
finding suggests the importance of the lower frequency range (1-2 kHz) of the MOC
efferent system’s involvement in the cocktail party neural processors as they pertain to
binaural hearing.
The first clue regarding the possible role of centrifugal pathways in
discriminations of signals in noise came from the work of Dewson in 1968. He trained
monkeys to pick out vowel sounds such as ‘I’ and ‘U’ presented to the animal in the
presence of white noise. He then measured the threshold of the discrimination between
these sounds in noise. Following surgical section of the crossed olivo-cochlear bundle at
the midline on the floor of the fourth ventricle, Dewson found a rise in masked threshold
of up to 15 dB. There is a possiblility therefore that other centrifugal pathways may also
be involved in ‘signal in noise’ discriminations.
Nieder and Nieder (1970) were likely the first to coin the term ‘anti-masking’
when they observed that efferent stimulation significantly increased neural response to
loud click in noise. Comis (1973) studied influence of atropine effect on the cochlear
nucleus on detection of signals in noisy background. Micheyl and Collet (1996) found a
possible relationship between detection of tones in noise and the strength of efferent
activation, as measured by contralateral suppression of otoacoustic emissions (Littman et
al., 1992; Williams et al., 1994; Maison et al., 1997).
Similar to Dewson’s (1968) finding, Heinz et al., (1998) showed that vowel
formant discrimination in cats was adversely affected by bilateral efferent section only in
12
high-level noise background but not at low noise levels. Giraud et al. (1997) were the
first clinical investigators to demonstrate efferent influences on human speech perception.
Of particular significance is the link they established between cochlear de-efferentation in
vestibular nerve neurectomized (VNT) patients and a loss of the ability to recognize
monosyllabic words in background noise. They showed that speech-in-noise
intelligibility is positively correlated with the strength of OAE suppression in normal
hearing humans. As a more direct test of the importance of efferent feedback in speech
processing, these investigators also found that unilateral VNT patients scored better in
speech-in-noise recognition tasks when stimuli were presented to the ear with intact
olivocochlear projections. Zeng et al., (2000) conducted behavioral studies in VNT
patients to evaluate anti-masking function proposed for the efferents. They found poorer
speech in noise recognition was observed in the surgery ear than the non-surgery ear, but
that finding was confounded by hearing loss. The present study using normal hearing
humans of different age shows that age-related difficulty understanding speech in
background noise is related to an age-related functional decline of the MOC efferent
system
Older adults are known to have significantly greater difficulty in recognizing
speech in the presence of background noise than young adults have (CHABA, 1988).
Although, in the main, sensorineural hearing loss contributes to the problems, absolute
pure tone thresholds are poor predictors for speech intelligibility in noise (Beattie et al.,
1997; Studebaker et al., 1997; Halling &Humes, 2000; Noorddhoek et al., 2001; Pittman
& Wiley, 2001). There are probably a number of age-related changes in both peripheral
13
and central auditory processing contribute to this difficulty (Gordon-Salant S, 1987;
Humes LE, 1996; Frisina DR and Frisina RD, 1997).
The present study shows that age itself is one of the important factors to affect
speech understanding in noise, consistent with the previous study (Kim et al., 2003).
Subjects in the old group in this study were selected on the basis of their relatively good
hearing. This was done to rule out any significant peripheral hearing loss. For example,
less than 10 % of subjects who are over the age of 60 years have less than 25 dB HL from
0.25 to 8 kHz. Therefore, the poor performance of speech understanding in noise by the
elderly generally, must consider the possible effect of central presbycusis.
V. SUMMARY and CONCLUSIONS
It is well known that older individuals have more difficulty in understanding
speech in background noise than young adults. Interestingly, a recent study shows that
the function of the MOC efferent system declines with age (Kim et al., 2002). The
present study investigated the relationship between the MOC efferent system and speech
understanding in noise in normal hearing humans of different ages. Our findings suggest
that (1) age-related difficulties in understanding speech in background noise are related to
the age-related functional decline of the MOC efferent system, (2) the higher frequency
(4-6 kHz) range of the MOC efferent function is correlated with speech processing when
the background noise and speech come from similar spatial locations (HINT N0), and (3)
the 1-2 kHz frequency range of the MOC efferent system is correlated with spatial RFM
based on binaural processing, i.e., cocktail party processor neural mechanisms. In
conclusion, our findings suggest that the auditory MOC efferent system might function as
14
a nonlinear adaptive filter during speech processing in background noise and also as a
cocktail party processor.
Acknowledgments
The authors would like to thank Prof. Jean Rouat, Prof. Jacqueline Walker, and Dr. Jiefu
Zheng for fruitful discussions and Dr. Arthur S. Hengerer for great support for study. The
work was supported by NIH Grant P01 AG09524 from the National Institute on Aging,
and the International Center for Hearing and Speech Research, Rochester NY, USA
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vestibular neurectomy subjects. Hearing Research 142, 102-112.
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Table 1. Age and sex distribution and thresholds of pure tone average (0.5, 1, and 2 kHz)
for three age groups
Group Age range N (female/male)
PTA average of both ears for HINT
PTA average of the target ear for CS (Right/Left)
Young 18-27 9 (5/4) 3.87 ± 2.37 SD dB HL 3.78 ± 1.76 SD dB HL (4/5)Middle-aged 41-49 6 (3/3) 5.97 ± 2.60 SD dB HL 5.83 ± 2.30 SD dB HL (4/2)Old 62-75 10 (5/5) 9.23 ± 4.02 SD dB HL 7.80 ± 3.76 SD dB HL (5/5)
Table 2. The results of contralateral suppression (CS) for three age groups (unit: dB).
Group CS in 1-6 kHz of f2 CS in 1-2 kHz of f2 CS in 4-6 kHz of f2 Young -0.82 ± 0.61 SD -1.01 ± 0.48 SD -0.54 ±0.89 SD Middle-aged -0.11 ± 0.13 SD * 0.08 ± 0.35 SD * -0.16 ± 0.59 SD Old 0.03 ± 0.52 SD ** -0.28 ±0.85 SD 0.40 ± 0.75 SD * One-way ANOVA F(2,22)= 7.51, p<0.01 F(2,22)=5.85, p<0.01 F(2,22)=3.63, p<0.05
Indicate, statistically significant effect:
* post-hoc t-test, p<0.05, re: young, ** post-hoc t-test, p<0.01, re: young.
Table 3. The results of speech intelligibility in HINT N0 and spatial RFM (unit: dB)
Group HINT N0 (SNR) RFM Young -2.67 ± 0.87 SD 5.14 ± 1.21 SD Middle-aged -2.78 ± 0.52 SD 4.23 ± 0.56 SD Old -1.76 ± 0.76 SD * 3.79 ± 1.57 SD One-way ANOVA F(2,22)=4.81, p<0.05 ns
Indicate, statistically significant effect:
* post-hoc t-test, p<0.05, re: young, ns; not significant
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Pure Tone Audiogram
Frequency (Hz)
.25 K .5 K 1 K 2 K 3 K 4 K 6 K 8 K
dB
HL
0
20
40
60
80
100
Young GroupMiddle Aged GroupOld Group
Fig. 1. Audiometric thresholds averaged for the right and left ears of the young adult
(black circles), middle-aged (grey circles) and old (open circles) groups. Error bars
indicate standard deviations. HL – dB of hearing level, K – kHz.
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CS of DPOAE at 4-6 kHz frequency range of F2
-3 -2 -1 0 1 2
HIN
T N
0 (d
B S
NR
)
-5
-4
-3
-2
-1
0
Young groupMiddle-aged group Old group
Fig. 2. Correlation between the speech intelligibility in noise at 0 degree azimuth, SNR of
HINT N0º, and CS of DPOAEs in the 4-6 kHz frequency range (f2). Pearson r=0.4295,
p<0.05. CS – contralateral suppression, DPOAE – distortion product otoacoustic
emission, SNR – signal-to-noise ratio.
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CS of DPOAE on 1-2 kHz frequency range of F2
-2.5 -2.0 -1.5 -1.0 -0.5 0.0 0.5 1.0 1.5
RF
M (
dB
)
1
2
3
4
5
6
7
8
Young groupMiddle-aged groupOld group
Fig. 3. Correlation between the spatial RFM and CS of DPOAE at 1-2 kHz frequency
range of f2. Pearson r=-0.4455, p<0.05. CS – contralateral suppression, DPOAE –
distortion product otoacoustic emission, RFM – release from masking.